Comparisons of topical and spray applications of two pesticides, triazophos and jinggangmycin, on the protein content in the ovaries and fat bodies of the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae)
Graphical abstract
Introduction
The brown planthopper (BPH) Nilaparvata lugens Stål, is a classic pest whose resurgence is induced by pesticides. The mechanisms of pesticide-induced resurgences of pests are involved in the stimulation of reproduction [1], [2], [3], [4] and the destruction of their natural enemies [5], [6]. Pesticides stimulate the reproduction of pests by increasing the protein and RNA content in the ovaries and fat bodies of adult females. The protein and RNA contents in the ovaries and fat bodies have been shown to increase linearly with insecticide concentrations and days after emergence (DAE) when three insecticides triazophos (TZP), deltamethrin and imidacloprid, were applied [7]. The genes associated with reproduction were up-regulated expressions [4], [8]. In addition, insecticides significantly enhanced the protein content (including sperms) of male accessory glands (MAGs) after 40 ppm TZP and 12 ppm deltamethrin treatments [8], [9]. For example, the protein content of MAGs after 40 ppm TZP and 12 ppm deltamethrin treatments was doubled compared with that of control males [10]. Interestingly, the effect of insecticides on the reproduction of BPH males can be transferred to females via mating [11]. Experiments showed that a greater quantity of MAG products of insecticide-treated adult males was transferred to adult females via mating [10] and resulted in an increase of the number of eggs laid of females [11]. Furthermore, changes in the biochemistry and physiology of rice plants induced by the foliar spray of pesticides also are one mechanism underlying the stimulation of BPH reproduction [1]. For example, foliar sprays of TZP, jinggangmycin (JGM; a fungicide), and imidacloprid significantly decreased the oxalic acid content of rice plants [12]. Rice plants treated with pesticides are beneficial to the feeding and survival of BPH [1]. In addition, whether pesticides stimulate BPH reproduction may depend on the treatment method. For example, the number of eggs laid by BPH females that have experienced JGM foliar sprays is significantly greater than that of eggs laid by BPH that have experienced a topical treatment [4]. Thus, the treatment methods have important implications for pests. The methods used in numerous pesticide toxicology experiments, including the pesticide-induced stimulation of reproduction, are either topical or spray tests. However, the effects of topical and foliar spray applications of pesticide on protein content of the ovaries and fat bodies in BPH have not been investigated.
Physiologically, the number of eggs laid is affected by the synthesis of yolk protein in the fat body. However, the yolk protein content is also influenced by nutritional and environmental conditions. Thus, the protein content in fat bodies of the adult females is a physiological index for the degree to which reproduction is stimulated by insecticides. Variation in the fat body and ovary proteins shows the same tend. Here, we compared the effects of two treatment methods (topical application and foliar spray) of two pesticides on the protein content of the ovaries and fat bodies in BPH.
We selected TZP and JGM not only because the organophosphate TZP is a classic insecticide that stimulates the reproduction of BPH [2], [3], [13], but also because recent studies have shown that TZP enhances the thermotolerance of BPH [14]. JGM, an antibiotic compound developed in China, is a fungicide that is mainly used to control the rice sheath blight Rhizoctonia solani in China. The fungicide is commonly applied two or three times during rice growth by foliar spray at the commercial rate of 125–175 g.a.i.ha−1 (approximately 200–300 ppm). The objective of this study was to compare the effects of different pesticide treatment methods on the protein content of the ovaries and fat bodies in BPH.
Section snippets
Rice variety, insects, and pesticides
The rice (Oryza sativa L.) variety Ningjing 2 (japonica rice) was used in each trial. This variety of rice was selected because it is commonly planted in Jiangsu Province, China. Seeds were sown outdoors in standard rice-growing soil in cement tanks (height 60 cm, width 100 cm, and length 200 cm). When seedlings reached the 6-leaf stage, they were transplanted into plastic pots (30 cm diameter, 30 cm height), with 4 hills per pot and 4 plants per hill. The rice plants used in the experiments were at
Effects of topical and spray treatments of TZP and JGM on protein content in the ovary of BPH
The ANOVA of the data presented in Fig. 1 showed that the pesticides and the treatment methods significantly influenced protein content in the ovaries of BPH (Table 1). Grand means (means of main effect) of protein content in the ovary at 2 and 3 DAE in the foliar spray treatments were significantly greater than those observed for the topical treatments, which increased by 23.9 (from 1.42 to 1.76) and 8.82% (from 4.42 to 4.81), respectively. For both pesticides, grand means of protein content
Discussion
Here, we showed that the foliar spray of TZP and JGM promoted the synthesis of protein in the ovaries and fat bodies of BPH females. The protein content in the ovaries and fat bodies after the spray treatment was significantly higher than that observed after the topical treatment, especially the spraying of JGM. The above findings have important implications for the study of the physiological and ecological mechanisms of pest resurgence and for pest management because foliar spraying is one of
Acknowledgments
This research was partially funded by The National Nature Science Foundation of China (31371938), the Ph.D. Advisor Fund of the Ministry of Education of China (No. 20123250110008), and Jiangsu Province Agricultural Fund for Independent Innovation (CX(14)2025).
References (20)
- et al.
Effects of different treatment methods of the fungicide jinggangmycin on reproduction and vitellogenin gene (Nlvg) expression in the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae)
Pestic. Biochem. Physiol.
(2012) - et al.
Relative toxicity of insecticides to rice planthopper and leafhoppers and their predators
Crop Prot.
(1986) - et al.
The combined effects of temperature and insecticide on the fecundity of adult males and adult females of the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae)
Crop Prot.
(2012) - et al.
Mating pair combinations of insecticide-treated male and female Nilaparvata lugens Stål (Hemiptera:Delphacidae) planthoppers influence protein content in the male accessory glands (MAGs) and vitellin content in both fat bodies and ovaries of adult females
Pestic. Biochem. Physiol.
(2010) - et al.
Insecticide-induced increase in the protein content of male accessory glands and its effect on the fecundity of females in the brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae)
Crop Prot.
(2010) - et al.
Two-way effect of pesticides on zeatin riboside content in both rice leaves and roots
Crop Prot.
(2004) Ovarian and fat body protein concentrations in Ips sexdentatus (Coleoptera:Scolytidae) parasitized by nematodes
J. Invertebr. Pathol.
(1984)- et al.
Pesticide-induced susceptibility of rice to brown planthopper Nilaparvata lugens
Entomol. Exp. et Appl.
(2001) - et al.
Cultivar and insecticide applications affect the physiological development of the brown planthopper, Nilaparvata lugens (Stål) (Hemiptera:Delphacidae)
Environ. Entomol.
(2008) - et al.
Comparisons of stimulatory effects of a series of concentrations of four insecticides on reproduction in the rice brown planthopper Nilaparvata lugens Stål (Hemiptera:Delphacidae)
Int. J. Pest Manag.
(2009)
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Silencing of triazophos-induced Hexokinase-1-like reduces fecundity in Nilaparvata lugens (Stål) (Hemiptera: Delphacidae)
2019, Pesticide Biochemistry and PhysiologyCitation Excerpt :The brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae), is a classic insecticide-induced resurgent pest throughout Asian rice-growing regions (Chelliah and Heinrichs, 1980). The resurgence of N. lugens induced by commonly used chemical agents has been well documented (Azzam et al., 2009; Ling et al., 2011; Wang et al., 1994; Yin et al., 2008), including fenvalerate, triazophos (TZP), detamethrin, methamidophos, and fungicide jinggangmycin (Bao et al., 2009; Jiang et al., 2012; Zhang et al., 2014; Zhu et al., 2014). Our previous work have described that several genes modulate N. lugens fecundity by probably operating in sugar homeostasis.
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2018, Pesticide Biochemistry and PhysiologyCitation Excerpt :TZP treatment enhanced flight capacity of BPH [32] as well as increase of reproduction, which was related to increase of energy in treated BPH. In addition, protein contents in ovaries and fat bodies in TZP-treated BPH were significantly higher than control group [33]. β-oxidation can oxidize fatty acids into CO2 and water releasing energy for reproduction and flight of organisms need via synthesis of ATP.
Pesticide-induced changes in fecundity and rice stripe virus transmission ability in Laodelphax striatellus (Homoptera: Delphacidae)
2017, Journal of Asia-Pacific EntomologyCitation Excerpt :The active ingredient in validamycin is a large water-soluble glucoside compound, which is unlikely to penetrate the wax layer of the insect cuticle. Zhu et al. (2014) showed that application of validamycin as a foliar spray stimulated the reproduction of N. lugens; however, topical treatments with the fungicide did not enhance fecundity. It is tempting to speculate that foliar sprays with validamycin induced changes beneficial for virus transmission in rice plants infested with naïve SBPH.
Lethal and sublethal effects of sulfoxaflor on the small brown planthopper Laodelphax striatellus
2016, Journal of Asia-Pacific EntomologyCitation Excerpt :Sublethal doses of insecticides stimulate insect fecundity are often observed, particularly in Hemiptera insects and in mites (Cohen, 2006). When brown planthopper female adults are exposed to LD3 of triazophos, protein synthesis is increased in ovaries and fat bodies (Zhu et al., 2014), which may subsequently increase the number of laid eggs. Zhang et al. (2015) observed similar results in the test of cyantraniliprole on Bactrocera dorsalis.
Jinggangmycin increases fecundity of the brown planthopper, Nilaparvata lugens (Stål) via fatty acid synthase gene expression
2016, Journal of ProteomicsCitation Excerpt :In particular, the JGM treatments led to increased expression of the BPH gene encoding vitellogenin [9]. Our related report documents the influence of foliar JGM sprays on ovarian protein content, foliar spray leading to about ↑ 73% at day 2 after emergence, compared to about 5% following topical application [10]. We reported similar results for fat body protein contents.